Asian Journal of Applied Science and Technology (AJAST) Volume 7, Issue 2, Pages 204-216, April-June 2023 Heavy Metals in Agricultural Soil and Their Impacts on Rice Production and Human Health: A Review Most. Serajam Monira & M.G. Mostafa* Water Research Lab, Institute of Environmental Science, University of Rajshahi, Rajshahi 6205, Bangladesh. Corresponding Author Email: mgmostafa@ru.ac.bd* DOI: https://doi.org/10.38177/ajast.2023.7222 Copyright: © 2023 Most. Serajam Monira & M.G. Mostafa. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Article Received: 23 April 2023 Article Accepted: 15 June 2023 Article Published: 25 June 2023 ABSTRACT Rice is one of the most important sources of carbohydrates for humans. The non-degradable and carcinogenic characteristics of heavy metals are the main concerns. Intensive use of farm inputs, industrialization and urbanization cause heavy metals accumulation in the soil, water, and rice grains. This review aimed to assess heavy metals pollution in agricultural soil and their transformation into rice grains. It collected information from different journals, websites, and published reports on heavy metals in soils, water, and accumulated rice grains in the last 13 years. The analysis results illustrated that the amount of heavy metal in the soil and rice of different rice-producing countries was higher than the permissible limits of the WHO, United Kingdom, Tianjin, and European Union standards. The accumulation of heavy metals in agricultural land has become a threat to humans as well as the environment. Reports showed that the higher concentrations of heavy metals in rice grains may cause heart disease, diabetes, possibly stroke, liver changes, hearing changes, changes in blood pressure, diarrhea, flushing of the face, etc. in humans. Regular monitoring and strict regulations of industrial discharge and chemical fertilizer should be recommended for the safety of soil and public health in rice-producing countries. Keywords: Accumulation; Concentration; Heavy metals; Industrial discharge; Humans; Public health; Rice; Soil. ░ 1. Introduction Rice is a staple food source for human consumption but grown in soil with contaminated irrigated water cause huge threats to humans. The main sources of heavy metals in soils are wastewater irrigation, solid waste disposal, sludge application, chemical fertilizers, and industrial activities (Tareque et al., 2023; Islam and Mostafa, 2023; Serder et al., 2020; Park et al., 2011; Arao et al., 2010; Ata et al., 2013; Keshav et al.,2016; Bilos et al., 2001; Chandra et al., 2011; Reddy et al., 2013; Chowdhury et al., 2015, 2013; Mukeeb et al., 2008; Fahmida et al., 2017; Domingo et al., 1983). Most of the industries are viewed to discharge their wastage on land or into surface water after partial treatment or without treatment (Monira et al., 2023; Shakil and Mostafa, 2021; Rahim and Mostafa, 2021; Islam and Mostafa, 2022; Jolly et al., 2012; Chowdhury et al., 2016; Chary et al., 2008. Olgun et al., 2012). Rice (Oryza sativa or Oryzaglaberima) serves as the main carbohydrate supplies more than half of the world’s population (IRRI 2001; Pearl. S, 2015: Yoneyma et al., 2015; Zhang et al., 2011). In 2014, global rice production reached 497 million tons, and was consumed 83% as food (FAO, 2014). In Asia alone, more than 2.3 billion people obtain 65 to 75 percent of their caloric intake from rice or rice products (FAO, 2002). Rice provides amino acids, vitamins, and minerals to consumers. In Asian areas, rice, the main alimentary crop, is susceptible to heavy metal pernicious due to the recurrent usage of excess water and metal-enriched agro-chemicals, which are responsible for the deposition of heavy metals inside the topsoil of the ponds (Fangmin et al., 2006; Department of Petroleum Resources, 2002; Emumejaye, 2014). Several research studies found serious metallic contamination of soil, water, and sediments (Islam and Mostafa, 2021a; Zakir et al., 2012, 2013, 2014, 2015; Kamal et al., 2016; Kumar and Seema, 2016; Bakali et al., 2014). Toxic metal levels hinder the metabolic processes of rice plants (Cai et al., 2010), which reduces yield. Chemical fertilizers (Bian et al., 2015; Nessa et al., ISSN: 2456-883X 204 Asian Journal of Applied Science and Technology (AJAST) Volume 7, Issue 2, Pages 204-216, April-June 2023 2014; Ahmed et al., 2010, 2016; Yasmin et al., 2019; Li et al., 2013) and pesticides (Habib et al., 2012; Shomar, 2006) may increase heavy metal concentrations in soils and plants. Contaminated localities in all aspects of the world are going to be a greater threat to crop plantations. Heavy metals influence almost all countries, but the extent of their severity varies greatly. Heavy metal concentrations in soils and rice plants indicate the threat of toxicity to the health of consumers (Kamani et al., 2018; Jhedioha et al., 2016; McDowell, 2003; Leo et al., 2005; Hu et al., 2014). So, it is essential to determine the toxic levels of heavy metals in agricultural soil and irrigation water. This review article aimed at assessing the heavy metal contamination of soil, their transformation into rice grains, and their effects on humans. ░ 2. Materials and Methods This study identified over 250 articles on rice production in contaminated soils published in different international peer-reviewed journals, but finally considered the most relevant 35 articles, mainly from rice-producing countries like Bangladesh, India, China, Macedonia and the Philippines. The papers were selected considering the rice produced in heavily metal-contaminated agricultural lands. Most of the industries discharge their effluent without or poorly treated into nearby lowland and or surface water bodies through a main drain. The agricultural lands adjacent to the water body are being irrigated, and the contaminated water threatens food safety and human health. Hence, the rice grains in these areas may be contaminated with heavy metals. ░ 3. Results and Discussions 3.1. Heavy metal standard in soil The World Health Organization (WHO), United Kingdom, Tianjin, and European Union Standards fixed the permissible limit of heavy metal concentration in soil (Table 1). Table 1. Permissible limits of heavy metal concentration in soil fixed by WHO and other organizations Heavy metals (mg/kg) → Country/ Organization ↓ Cd Zn Cu Cr Pb Ni As Hg References Denneman and Robberse 1991; Ministry of Housing, Netherlands 1994 Ediene et al., 2017 WHO 0.8 50 36 100 85 35 - - United Kingdom 1.4 - 63.0 6.4 70.0 - - - Tianjin Standard, China (2nd grade) 0.159 115 43.71 107D 124P 32.83 - 16.64P* 14.64D* 0.258 Zuwei et al., 2015 European union standard (EU2002) 3.0 300 140 150 300 - - - Zuwei et al., 2015 D: upland soil, P: paddy soil ISSN: 2456-883X 205 Asian Journal of Applied Science and Technology (AJAST) Volume 7, Issue 2, Pages 204-216, April-June 2023 Table 1 shows that the heavy metals contamination levels fixed by the WHO is lower than that of other organizations. The World Health Organization (WHO), the Tianjin standard, and the European standard fixed the permissible limit for rice fields. The European Standard, which has a fixed Cd permissible limit of 3.0 mg/kg (Zuwei et al., 2015), was the highest, and the Tianjin Standard, China (2nd grade), is fixed at 0.159 (Zuwei et al., 2015), which was the lowest among the standards. The European Union standard (EU 2002) fixed the Cu concentration at 140 mg/kg (Zuwei et al., 2015), which is approximately three times higher than permissible limit of the WHO (36 mg/kg) (Denneman and Robberse, 1991; Ministry of Housing, the Netherlands, 1994). The European Union standard (EU 2002) fixed the Pb limit at 300 mg/kg (Zuwei et al., 2015), which is approximately 9 times higher than the lower limit of 32.83 mg/kg fixed by the Tianjin Standard, China (2nd grade) (Zuwei et al., 2015). The Tianjin Standard, China (2nd grade), fixed the Hg limit at 0.258 mg/kg, but the other organizations have no standard limit for this element. The organizations fixed the permissible limit of heavy metals in soils, which is helpful for building sustainable soils and agricultural management. 3.2. Heavy metal concentration in soil Heavy metals were determined in industrial areas (Savar, Gazipur, Ashulia) of Bangladesh, the Philippines (Solana, Cagayan Valley, Sta. Cruz, Zambales, Central Luzon, Sta. Rosa City, Laguna), China (Hunan Province), India (East Coast), and Macedonia (Kocani Field). In Bangladesh, three major industrial areas are Savar, Gazipur, and Ashulia. Most of the industry discharges its untreated effluent into the soil, which is then transferred to crops and accumulated in edible grains. The study shows that the Fe concentration was found to be 976.12 mg/kg in the Ashulia area, which was higher than the Savar area (873.61 mg/kg) and Gazipur (668.32 mg/kg). The concentration of Cu (31.54 mg/kg) in the Savar area was higher than that in the Gazipur (19.76 mg/kg) and Ashulia (29.65 mg/kg) areas, while the Cd concentration (18.56 mg/kg) was the highest among the other two areas. Concerning Cr (46.93 mg/kg) and Co (43.09 mg/kg) concentrations, they were highest in the Savar and Ashulia areas, respectively, among the three areas of Bangladesh. The AS (3.76 mg/kg) in Ashulia was higher than the others (Table 2). All the concentrations of heavy metals exceeded the standard limits of the WHO (Table 1). In the Philippines, three important rice-producing areas are the Solana and Cagayan Valleys. Sta. Criz, Zambales, Central Luzon Sta. Rosa City, B. Laguna The Cu content in soil was almost double in Sta. Rosa City, Laguna (115.9 mg/kg) due to the location near urban areas with urban waste than in Solana, Cagayan Valley (53.3 mg/kg), where in Sta. Cruz, Zambales, Central Luzon (<25.0 mg/kg), the Cu content of Sta. Rosa City, Laguna (115.9 mg/kg), Solana, Cagayan Valley (53.3 mg/kg) was higher than the permissible limits of the WHO (36mg/kg), the Tianjin standard (43.71mg/kg) (Table 1). Cr content in Sta. Cruz, Zambales, Central Luzon (1126.5 mg/kg), which is almost 31 times higher than Solana Cagayan Valley (36.6 mg/kg) and Sta. Rosa City (36.8 mg/kg), Cr content of Sta. Cruz, Zambales, Central Luzon was more alarming than the limit of the WHO (100 mg/kg), the Tianjin Standard (107D, 124P), and the European Union standard (150 mg/kg) (Table 1). Ni content is 2624.1 mg/kg in Sta. Cruz, Zambales, and Central Luzon, is 52 times higher than in Solana, Cagayan Valley, and Sta. Rosa City (<50.0 mg/kg). The Ni content in Sta. Cruz, Zambales, Central Luzon were alarming compared to the WHO (35 mg/kg) and the United Kingdom (100) (Table 1). In China, Cd concentration was 1.40 mg/kg, which was higher than the ISSN: 2456-883X 206 Asian Journal of Applied Science and Technology (AJAST) Volume 7, Issue 2, Pages 204-216, April-June 2023 WHO (0.8 mg/kg) and the Tianjin standard (0.159 mg/kg), and Ni concentration was 33.9 mg/kg, which was higher than the WHO (35 mg/kg) and the United Kingdom (100.0 mg/kg). The concentrations of Hg and Pb were 14.9 and 51.4 mg/kg, respectively, which were higher than the Tianjin standard (0.258 and 32.83 mg/kg) (Table 1).In India, Zn concentration was 3.8–33.8 and Pb concentration was 5.3–19.8, which was lower than the permissible limits of the WHO, the Tianjin standard, and the European Union (Table 1). In Macedonia, Cd concentration was 0.9 mg/kg, which was higher than the WHO (0.8 mg/kg) and the Tianjin standard (0.159 mg/kg), Zn was 206 mg/kg, which was higher than the WHO (50 mg/kg) and the Tianjin standard (115 mg/kg), and Pb was 128 mg/kg, which was higher than the WHO (85 mg/kg) and the Tianjin standard (32.83 mg/kg) (Table 1). The study observed that Cu (115.9 mg/kg) concentration was higher in Sta. Rosa City, Laguna, Philippines, than in the other countries. Cd (18.56 mg/kg) was highest in the Ashulia area of Bangladesh, Cr (1126.5 mg/kg) was highest in Sta. Cruz, Zambales, Central Luzon, the Philippines, and Hg (14.9 mg/kg) and Pb (51.4) levels were found to be highest in Hunan Province, China. The results showed that the Cd concentrations in the soil of Bangladesh, the Philippines, China, and Macedonia exceeded the standard permissible limits set by the WHO and other organizations (Tables 1 and 2). The Cr concentration in the Philippines (Sta. Cruz, Zambales, and Central Luzon) was the highest among the countries that exceeded the permissible limits. The study observed that heavy metal concentrations in agricultural fields were found to be higher due to anthropogenic activities in different countries. Table 2. Average concentration of heavy metal in soil of rice producing Countries Heavy metal (mg/kg) Fe Cu Cd Cr Co As Hg Ni Zn Pb Area 873.61 31.54 14.98 46.93 28.65 3.32 - - 78.65 38.07 Savar Bangladesh 668.34 19.76 11.08 40.76 9.56 2.98 - - 64.98 42.78 Gazipur 976.12 29.65 18.56 34.87 43.09 3.76 - - 81.9 34.09 Ashulia - 53.3 <10.9 <36.8 - <9.0 <7.0 <50.0 44.3 >8.0 - <25.0 <10.0 1126.5 - <9.0 >8.0 2624.1 <15.0 >8.0 - 115.9 <10.0 <36.8 - <9.0 <7.0 <50.0 81.2 16.2 China - - 1.40 27.2 - - 14.9 33.9 - India - - 0.02-0.6 1.3-7.8 - - - - Macedonia - 33 0.9 - - - - - References Country Philippines Hasan et al., 2022 Solana, Cagayan valley Sta. Cruz, Zambales, Central Luzon Sta. Rosa City, Laguna Sanchez et al., 2015 51.4 Hunan province Zeng et al., 2015 3.8-33.8 5.3-19.8 East coast Satpathi et al., 2014 206 128 Kocani field Rogan et al., 2009 ISSN: 2456-883X 207 Asian Journal of Applied Science and Technology (AJAST) Volume 7, Issue 2, Pages 204-216, April-June 2023 Table 3. Standard level of heavy metal concentration in rice grain Heavy metal (mg/kg) As Cd Cu Pb Zn 0.5 0.2 10 0.2 50 References Country Chinese standardized value International standardized value Kong et al., 2018 0.2 0.4 - 0.2 - *Permissible limit of heavy metal in rice grains in the National Food Safety Standard of the People’s Republic of China (GB 2762-2017) and the Agricultural Industry Standards of the People’s Republic of China (NY 861-2004). From the Codex Alimentarius Commission (CAC) Standard Codex Stan 1993-1995 adopted in 1995; revised in 1997, 2006, 2008, and 2009; amended in 2010, 2012, 2013, and 2014. 3.3. Heavy metal concentration in rice grain of different countries Table 4 shows the concentration of heavy metals in rice in different areas of Bangladesh, the Philippines, China, India, and Macedonia. This study illustrated that in Bangladesh, the Cd concentration in rice was found to be highest (1.61 mg/kg) in Ashulia among the three areas of Bangladesh, while the Cu concentration in rice was highest in the Savar area (38.12 mg/kg). Concerning Cr (23.67 mg/kg) concentration, rice in the Ashulia area showed the highest level among the three areas of Bangladesh. The study observed that heavy metals may be transported to rice grains due to the industrial discharge of waste and wastewater onto the surface. The concentrations of the above elements exceeded the standard permissible limits for rice grains, indicating human health hazards (Table 3). However, As and Zn concentrations were lower than the permissible limit. In the Philippines, Solana, Cagayan Valley, Sta. Cruz, Zambales, and Sta. Rosa City was selected for this study. In these areas, Cu, Cr, As, Ni, and Pb content were the same, and Zn was higher (68.6 mg/kg) in Solana, Cagayan Valley than in Sta. Cruz, Zambales, Central Luzon (17.0 mg/kg), and Sta. Rosa City, Laguna (55.7 mg/kg). All the heavy metal content was higher than the standard level (Table 3). In China, Cd content was 0.312 mg/kg, Cr was 0.106 mg/kg, Ni was 0.59 mg/kg, Hg was 0.069 mg/kg, and Pb content was 0.023 mg/kg. In Macedonia, Cu content was 3.0 mg/kg, Cd was 0.069 mg/kg, As was 27.86 mg/kg, and Pb was 0.196 mg/kg. The Cu (38.12 mg/kg) concentration in rice at Savar, Bangladesh, was the highest among the countries (Table 4), which was far above the permissible limit (Table 3). Cd (<10.0 mg/kg) and Pb (<8.0 mg/kg) concentrations in Solana, Cagayan Valley, Sta. Cruz, Zambales, Central Luzon, and Sta. Rosa City, Philippines, was the highest among the countries (Table 4) and the permissible limit (Table 3). 3.4. Effect of heavy metal on human health Rice is considering as the most important grain for human nutrition and calorie intake. After consuming contaminated rice grains, they form bio-toxic compounds that mutilate their structures and cause health hazards. The study showed that several heavy metals were present in the rice grains on agricultural lands around industrial areas in different countries, posing a threat to human health. A discussion on how heavy metals in rice may cause harm to humans. ISSN: 2456-883X 208 Asian Journal of Applied Science and Technology (AJAST) Volume 7, Issue 2, Pages 204-216, April-June 2023 3.4.1. Arsenic (As) Arsenic is a tasteless and odorless metal. Arsenic present in higher-level at food can affect the pulmonary nervous system and skin and can cause cancer of the respiratory tract, peripheral neuropathy, and perforation of the nasal septum (Islam and Mostafa, 2021b; Mahurpawar, 2015; Zhou et al., 2008, 2016). Lower-level exposure can cause severe hazards, including nausea and vomiting, production of blood cells and vessels, abnormalities in heart rhythm, etc., and long-term low-level exposure can cause a darkening of the skin and the appearance of small corns or warts on the palms, soles, and torso (Martin S. et al., 2015; WHO, 1989, 1993, 1996, 1997; Jolly et al., 2016). 3.4.2. Cadmium (Cd) Cadmium is a very toxic metal. It affects Renal and Skeletal Pulmonary. It causes diseases like proteinuria, one of the most important signs of kidney damage, Glucosuria occurs when the urine contains more glucose than it should, Osteomalacia (characterized by the softening of the bones), Aminoaciduria, it occurs when the amount of amino acids increases greatly, emphaysemia, it causes shortness of breath (Mahurpawar M. 2015; Garcia et al., 1998; Engwa et al., 2019.).CD causes diarrhea and affects the lung (Martin S. et al., 2015; Deflora et al., 1997; Sobha et al., 2007). 3.4.3. Chromium (Cr) Chromium affects the lungs and causes ulcers, a discontinuity or break in a bodily membrane, and perforation of the nasal septum, which occurs most commonly along the anterior cartilaginous septum (Mahurpawar M., 2015; Zhuang et al., 2009; Wang et al., 2005). Table 4. Average concentration of heavy metal of rice in different rice producing country Heavy metal (mg/kg) Fe Cu Cd Cr Co As Hg Ni Zn Pb Area 14.89 38.12 1.43 19.78 12.08 0.075 - - 121.76 1.21 Savar 9.49 25.34 0.98 11.54 8.54 0.031 - 0.18 107.43 - Gazipur 11.87 19.74 1.61 23.67 18.11 0.048 - - 97.34 1.32 Ashulia - <25.0 <10.0 <36.8 - <9.0 - <50.0 68.6 <8.0 - <25.0 <10.0 <36.8 - <9.0 - <50.0 17.0 <8.0 - <25.0 <10.0 <36.8 - <9.0 - <50.0 55.7 <8.0 China - - 0.312 0.106 - - 0.069 0.591 - 0.023 India - - 0.02-0.05 0.1-0.6 - - - - 3.2-7.2 0.01-1 East coast Macedonia - 3.0 0.069 - - - - - 27.86 0.196 Kocani field References Country Bangladesh Philippines Solana, Cagayan Valley Sta. Cruz, Zambales, Central Luzon Sta. Rosa City, Laguna Hunan province Hasan et al., 2022 Sanchez et al., 2015 Zeng et al., 2015 Satpathi et al., 2014 Rogan et al., 2009 ISSN: 2456-883X 209 Asian Journal of Applied Science and Technology (AJAST) Volume 7, Issue 2, Pages 204-216, April-June 2023 3.4.4. Manganese (Mn) Manganese is a metal usually found in combination with iron in minerals. It attacks the nervous system and causes central and peripheral neuropathies and muscle weakness in different parts of the body (Mahurpawar, 2015; Wang et al., 2005; Jolly et al., 2016). 3.4.5. Lead (Pb) Lead attacks the nervous system, hematopoietic and renal systems. Encephalopathy, it alters the function of brain function or structure (Islam and Mostafa, 2021c; Mahurpawar M., 2015). Lead causes anemia and kidney damage (Martin S. et al. 2015). 3.4.6. Nickel (Ni) Nickel is a toxic heavy metal. The presence of nickel in food grains can attack the nervous and pulmonary systems, causing visual defects, EEG changes, and pneumoconiosis, an interstitial lung disease (Mahurpawar, 2015; Wang et al., 2005; Jolly et al., 2016). 3.4.7. Mercury (Hg) Mercury attacks the nervous system and the renal system and causes proteinuria (Mahurpawar, 2015; Wang et al., 2005; EPA 2018). ░ 4. Conclusion This review observed that the Cu concentration (115.9 mg/kg) was higher in the soil of Sta. Rosa City, Laguna, Philippines, is located near the urban waste dumping area. The Cd and Cr concentrations were found to be higher (18.56 and 46.93 mg/kg, respectively) in the Ashulia and Savar industrial areas of Bangladesh, indicating industrial discharge caused heavy metal pollution in soils. The review also observed that Hg concentrations (14.9 mg/kg) in soil were higher in the Hunan Province of China as it was a mining area, and the Pb (128 mg/kg) concentration in Kocani Field, a municipality in the eastern part of North Macedonia, indicated heavy metal pollution in soil was the result of anthropogenic activities. The highest concentrations of Cu (38.12 mg/kg) and Zn (121.76 mg/kg) were found in rice grains in the Savar industrial area of Bangladesh. Concerning the concentrations of other heavy metals like Cd, Cr, As, Ni, and Pb in rice at Solana, Cagayan Valley, Sta. Cruz, Zambales, Central Luzon, Sta. Rosa City, and Laguna, Philippines, were found to be higher. This review observed that heavy metal toxicity concerns the world's agricultural sector, is intensified by industrialization, intensive use of farm inputs, and urbanization, and poses a threat to human health. The review showed that heavy metal concentrations in agricultural fields were found to be higher due to anthropogenic activities. The accumulation of heavy metals in rice grains transported from the soil makes the rice toxic for human consumption. People should be conscious of not cultivating rice near industrial waste discharge areas. The industry should dispose of its waste while considering environmental safety and sustainability. The government should take initiatives for awareness-building programs through the newspaper and television and knowledge-based curriculums for primary and secondary education to reduce surface water pollution. Now it is time to formulate the necessary rules and regulations for irrigation water. ISSN: 2456-883X 210 Asian Journal of Applied Science and Technology (AJAST) Volume 7, Issue 2, Pages 204-216, April-June 2023 Declarations Source of Funding The study has not received any funds from any organization. Competing Interests Statement The authors have declared no competing interests. Consent for Publication The authors declare that they consented to the publication of this study. The work has been submitted for publication with due consent of authorities of their institute. Authors’ Contributions All the authors equally participated in research and drafting of the manuscript. Acknowledgement Most. Serajam Monira would like to thank the Institute of Environmental Science, University of Rajshahi, Rajshahi, Bangladesh, for giving her a fellowship. References Ahmad and M.A. Goni (2010). Heavy metal contamination in water, soil, and vegetables of the industrial areas in Dhaka, Bangladesh. Environmental Monitoring and Assessment, 166(1–4): 347–357. doi: https://doi.org/10.1007/s 10661-009-1006-6. Ahmed, A.N.M. Fakhruddin, M.T. Imam (2016). Spatial distribution and source identification of heavy metal pollution in roadside surface soil: a study of Dhaka Aricha highway, Bangladesh. 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